The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group

Abstract

The collective behaviour of social groups is often strongly influenced by one or few individuals, termed here ‘keystone individuals’. We examined whether the influence of keystone individuals on collective behaviour lingers after their departure and whether these lingering effects scale with their tenure in the group. In the social spider, Stegodyphus dumicola, colonies' boldest individuals wield a disproportionately large influence over colony behaviour. We experimentally manipulated keystones' tenure in laboratory-housed colonies and tracked their legacy effects on collective prey capture following their removal. We found that bolder keystones caused more aggressive collective foraging behaviour and catalysed greater inter-individual variation in boldness within their colonies. The longer keystones remained in a colony, the longer both of these effects lingered after their departure. Our data demonstrate that, long after their disappearance, keystones have large and lasting effects on social dynamics at both the individual and colony levels.

The Achilles' heel hypothesis: misinformed keystone individuals impair collective learning and reduce group success

“…Taken together, these results suggest that keystone individuals have the propensity to become 'Achilles' heels' for their societies, leading to enhanced group vulnerability (under some conditions) because of their propensity to diminish societal performance when they harbour inaccurate information. Notably, in S. dumicola, as in other systems, an individual's probability of becoming a keystone individual is linked with its personality type [31,34]. This further highlights the value of considering individual variation in behaviour when exploring collective outcomes.…”

“…However, the effects of misinformation merely depend on the phenotypes (and the social influence) of the individuals that initially harbour it. In S. dumicola, as in some other systems [14,33], individuals' probability of emerging as a keystone individual is tightly linked with their personality type [31,34]. This provides further rationale for considering individual variation in personality in any complex society.…”

“…Links between personality and probability of becoming keystone individuals are fairly common [14,33]. In S. dumicola, the link between boldness and keystone-ness is particularly strong (R 2 ¼ 0.36-0.67) [30,31]: simply adding one very bold individual to a colony increases the number of attackers that respond to live prey by 300-600% and increases the mass gained by societies as a whole by 300%, and these effects linger for weeks after a keystone individual's removal [34]. No such effects are observed when the presence of shy individuals is manipulated.…”

“…act as keystone individuals) by catalysing aggressive foraging behaviour in their otherwise shy colony mates [31,34]. The longer that keystone individuals remain in a group, the more dramatic their effects become and the longer their effects linger following their departure or death [34].…”

Individual differences in boldness influence patterns of social interactions and the transmission of cuticular bacteria among group-mates

“…In colonies of S. dumicola, the execution of collective behaviours such as prey capture [33][34][35][36] and antipredator defences [37] is associated with heterogeneity among individuals in their boldness, suggesting that boldness is a reliable indicator of individuals' role in these societies. Therefore, we examined assortativity according to boldness by observing marked individuals in experimental colonies.…”